Funky Worms Cause Ants to Mimic Fruit

A normal giant gliding ant (left) and an infested ant (right). The red color of the gaster is not caused by a pigment, but thinning of the exoskeleton combined with the color of the nematode eggs. From Yanoviak et al, 2008.

In one of my favorite episodes of the animated TV show Futurama, the chief protagonist – delivery boy Philip J. Fry – becomes infested with worms after eating a dodgy egg-salad sandwich purchased from the restroom of an interstellar truck stop. Lucky for Fry, the parasites are beneficial – they repair his injuries and greatly enhance his cognitive abilities. (“Of all the parasites I’ve had over the years,” Fry explains to his coworkers, “these worms are among the… – hell! They are the best!”) The giant gliding ants (Cephalotes atratus) of Central and South American rainforests are not so fortunate. They, too, often become infested with a peculiar kind of worm, but these worms trigger a startling metamorphosis which transforms the ants into walking transports for the next generation of nematodes.

Naturalists have long recognized the ability of parasites to influence the behavior of their hosts. Among ants, especially, almost everyone has heard of the fungus Cordyceps unilateralis which causes “zombie” ants to climb up high and clamp down on a branch before the fungal stalk erupts from the back of the ant’s head. A previously unknown species of nematode worm – mentioned by scientists S.P. Yanoviak, M. Kaspari, R. Dudley, and G. Poinar Jr. in the April 2008 issue of The American Naturalist – also changes the attributes of its ant hosts, but in a very different way.

While studying giant gliding ants in the forests of Panama in May of 2005, the authors of the study noticed that the gasters (the bulbous, terminal part of the ant abdomen) of some individuals were bright red in color and held conspicuously high. This condition was first described in these ants over a century ago – they were even proposed to be a distinct type of ant in 1894 because of it – but no one knew what caused it. Yanoviak and colleagues found the answer. When they opened up the gasters of these ants they found hundreds of tiny, transparent eggs with tiny nematode worms inside. Closer inspection showed that the worms were a species hitherto unknown to science – a tetradonematid nematode similar to species which infest flies and beetles, but causing physical changes never before seen in an arthropod.

An infested ant photographed next to the fruits of Hyeronima alchorneoides. From Yanoviak et al, 2008.

Through observations of four infested colonies in the field and tests in the lab, the scientists were able to determine that the worms were using the ants to further their life cycle. As the researchers initially observed, the gaster of an infested ant will turn red (due to a thinning of the exoskeleton which looks red when combined with the nematode eggs), be held high almost constantly, and is easily detached from the rest of the body. The ants are also docile and sluggish; they fail to bite or give off alarm pheromones when faced by a threat.

The docility of the ants and their bright-red gasters make them easy targets for birds, the next essential part of the nematode life cycle. Birds have not been directly observed to consume these ants, but as the researchers found when they presented infected ant gasters and different colored clay balls to birds in the field, birds were highly attracted to what they perceived to be red or pink colored berries, and a test with a captive chicken showed that the nematode eggs could survive going through the bird digestive system. This was important, as the ants regularly pick up bird feces as they forage, making it relatively easy for an avian carrier to leave feces at a distant site where a different ant nest will pick up the feces (and hence the parasites).

It is not the adult ants which initially become infested, though. An internal filter-like organ prevents the nematode eggs from passing far enough to become established in their bodies. Instead, the colonies become infested when workers feed the bird feces to larvae in the nest. The juvenile nematodes take up residence inside the larvae, stunting the young ant’s growth (infested ants are about 10% smaller than healthy ones), and from there the worms grow and mate. The male worms die, but the females lay eggs in the gaster of the ant, and it is about this time that the host ants are switching from working in the nest to foraging outside the nest, a time when the ants will be susceptible to predation by birds.

As the authors note, there are at least two alternatives to this scenario.

1) It may be that the bodies of dead infested ants are being fed back to the colony, thereby continuing the nematode lifecycle. For the parasite to spread to new colonies, however, queens carrying the nematodes would have to successfully establish nests in new areas (unlikely if the nematodes suck resources from the ant and weaken them), or infested ants would have to be enslaved by neighboring colonies. The authors did not find direct evidence to support either idea.

2) The parasite may cause infested ants to be more conspicuous to animals which are already consuming ants on a regular basis. Birds seem to avoid healthy giant gliding ants because of their spiny armor and strong pheromones, but lizards and anteaters may not be so picky. In this case, these other vertebrates may pick out the infested ants as these individuals would be easier to spot, but this creates a problem with droppings. The feces of lizards and anteaters would be more likely to drop to the forest floor where they would be picked over by other species of ants, and so deprive the parasite of getting back into a giant gliding ant nest.

Further laboratory and field observations will be required to test the hypothesis presented in the American Naturalist paper, but, at present, predation by birds appears to best explain the modifications to the ants, the infestation of larvae by the parasite, and the dispersal of the nematode to new colonies. The details of how this two-host system evolved and the physiological mechanisms which trigger the changes in the ants are as yet unknown, but hopefully further research will help to explain how a tiny worm can so drastically change the appearance and behavior of an organism.